The impact of over-distraction on adjacent segment pathology and cage subsidence in anterior cervical discectomy and fusion

Over-distraction has been shown to be a risk factor for cage subsidence and postoperative neck pain after anterior cervical discectomy and fusion (ACDF). Biomechanical studies have demonstrated increased adjacent segment intradiscal pressure after ACDF. The purpose of this study is to determine if over-distraction of the index disc has an effect on adjacent segment pathology. A consecutive series of 145 patients who received primary ACDF for cervical degenerative pathologies from January 2010 to December 2017 were retrospectively reviewed. The patients were divided into: (1) Over-distraction group (postoperative–preoperative index disc height ≥ 2 mm), and (2) No-distraction group (postoperative–preoperative index disc height < 2 mm). Outcome measures included radiographic parameters, Japanese Orthopaedic Association (JOA) score, and incidences of cage subsidence, radiological and clinical adjacent segment pathologies (RASP and CASP) were compared between the two groups preoperatively, postoperatively, and at the final follow-up. The two groups were comparable with respect to age, follow-up length, JOA score, incidence of CASP, and radiographic parameters. The Over-distraction group (83 patients; 115 levels) had smaller preoperative index disc height (4.5 vs. 5.2 mm, p < 0.001), but taller postoperative index disc height (7.7 vs. 6.6 mm, p < 0.001) than No-distraction group (62 patients; 90 levels) Furthermore, significantly higher incidences of cage subsidence (47% vs. 31%, p = 0.04) and RASP (any progression: 48% vs. 15%, p < 0.001; progress ≥ 2 grades: 25% vs. 7%, p = 0.001) were observed in the Over-distraction group. The multivariate analysis indicated that over-distraction and multilevel fusion were independent risk factors for RASP. There were no clinical outcome differences between the Over-distraction group and the No-distraction group in ACDF. Over-distraction of the index level of ≥ 2 mm should be avoided because it significantly increases the incidences of RASP and cage subsidence.

Anterior cervical discectomy and fusion (ACDF) has been proven to be a safe and effective treatment for cervical degenerative pathologies since its first introduction by Smith and Robinson 1 .With consistent clinical results and surgical prognosis, the procedure includes complete removal of the disc materials and protruding osteophytes, and replacement with autologous bone grafts, allografts, interbody spacers, or a combination of these.Various materials have been applied as interbody spacer.Polyetheretherketone (PEEK) cages have been widely applied due to good biocompatibility and radiolucency allowing fusion assessment 1,2 .On the other hand, porous tantalum trabecular metal (TM) cages are famous of high porosity and biomechanical similarity of elastic modulus to bone 3,4 .Other materials of interbody spacer were also applied but not in our study.The elastic modulus of carbon fiber composite frame cages are close to bone, which helps to decrease the stress shielding and to promote bony fusion as described in Wolff 's law 5 .Titanium cage subsidence with the collapse of disc height and kyphotic deformity had been observed in previous study 6 .

Surgical techniques
After introduction of general anesthesia and endotracheal intubation, patients were placed in the supine position with the neck in mild extension.Target vertebral bodies were exposed via a standard Smith-Robinson anterior cervical approach.The operative levels were checked by intraoperative portable X-ray.A Casper distractor was applied for distraction of the vertebral bodies.All disc materials, including the herniated fragments, posterior osteophytes, and ossification of posterior longitudinal ligament (OPLL) were then removed under the assistance of a surgical microscope.The vertebral endplates were prepared with meticulous curettage to avoid endplate damages.Adequate neural decompression was confirmed through partial removal of the posterior longitudinal ligament.
The cages were packed with artificial bone substitutes, such as tricalcium phosphate, and/or demineralized bone matrix (DBM), and/or morselized allograft.After trials of size selection, the cages were inserted into the disc space.All patients wore a cervical collar for 6 weeks postoperatively.

Assessment of results
All patients received clinical and radiographic evaluations before surgery, immediate after surgery, and 6 weeks, 3, 12, 24 months after surgery until the last follow-up.Successful fusion was defined as the presence of bridging trabecular bone, or a < 2 mm distance change of the index level spinous process tips in plain radiographs dynamic series.Radiological adjacent segment pathology (RASP) was assessed on plain radiograph findings according to the grading proposed by Hilibrand et al. 7 , and modified by Chung et al. 17 .Table 1 presents the grading system for RASP, which is divided into six grades.All patients with symptoms related to cervical spine, including neck pain, arm pain, cervical myelopathy symptoms or other radiculopathy symptoms were arranged MRI at outpatients department to check if there are progressive adjacent segment pathologies or not.Patients with symptoms correlated to MRI findings of adjacent segment pathologies were diagnosed with clinical adjacent segment pathology (CASP).Cage subsidence was defined as a loss of index level disc height > 3 mm as compared to the height measured on the immediate postoperative radiographs 10 .The Japanese Orthopedic Association (JOA) scores for cervical spine were evaluated before and after surgery, and at the final follow-up.Radiographic parameters measured on plain radiographs before and after surgery, and at the final follow-up included index level disc height, and the heights of the cranial adjacent and caudal adjacent levels, local Cobb angle at the index level.Other measurements included cervical sagittal parameters including C2-C7 cervical lordosis (CL), T1 slope (TS), T1 slope minus cervical lordosis (TS-CL), neck tilt, thoracic inlet angle, and cervical sagittal vertical axis (cSVA).Two spine fellows evaluated each radiograph separately and made their own interpretations.The averaged measurements were set as final results for continuous data like disc height or Cobb angle.For categorical data, similar opinions between the two spine fellows were directly recorded as final results.The senior surgeon was consulted for final decision if the opinions were different between the two spine fellows.

Statistical analysis
Previous study showed interbody height increases 2.2 mm in high torque group and 1.9 mm in low torque group 18 .Recent biomechanical study had reported that larger-sized interbody cages (the height of ≥ 2 mm of the index disc height) could result in remarkable variations in biomechanical responses of adjacent levels 19 .To evaluate the effect of over-distraction, the patients were divided into two groups: (1) Over-distraction group (postoperative index disc height-preoperative index disc height ≥ 2 mm), and (2) No-distraction group (postoperative index disc height-preoperative index disc height < 2 mm).Patient demographic data and outcome measures were analyzed and compared between the two groups.Statistical differences between the two groups were calculated using the independent T test and the chi-square test.Risk factors of progression of RASP were determined by univariate and multivariate binary logistic regression analysis.A p value < 0.05 was considered statistically significant.Receiver operator characteristic (ROC) curves and the corresponding area under the curve (AUC) were used to evaluate how the prediction model of RASP preformed.All statistical analyses were performed using SPSS version 25 software (IBM-SPSS, Armonk, NY).

Data demographics
A total of 265 patients underwent ACDF between 2014 and 2016 were reviewed and the review process was showed in Fig. 1.There were 17 patients underwent the surgery for non-degenerative diseases and 8 patients were revision cases.Sixty-six patients were excluded for anterior plating and fifteen patients chose cervical disc prosthesis.For minimum 2 years follow-up, 14 patients were excluded.Finally, a total of 145 patients (88 males, Table 1.Radiological adjacent segment pathology (RASP) grading on plain radiographs.*The grading system was proposed by Hilibrand et al. 7 and modified by Chung et al. 17 .

Comparisons of outcome between the two groups
There were 83 patients included in the Over-distraction group and 62 in the No-distraction group.The age, number of fused levels, follow-up length, and fusion rate were comparable between the two groups (Table 2).The incidence of RASP was significantly higher in the Over-distraction group (48% vs. 15%, p < 0.001).In addition, the incidence of moderate progression of RASP (≥ 2 grades) was greater in the Over-distraction group (21% vs. 4%, p = 0.001).
All seven cases of CASP were in the Over-distraction group and the incidence was significantly higher than the No-distraction group (8% vs. 0%, p = 0.02).Figure 2 showed one case who underwent C4-5-6 ACDF with PEEK cage suffered from CASP 5 years after the operation.There were three patients received revision surgery after primary ACDF within follow up.Two of the patients suffered from pseudoarthrosis and one of the patients suffered from severe clinical adjacent segmental pathology.
The incidence of cage subsidence (disc height loss > 3 mm) was significantly higher in the Over-distraction group than the No-distraction group (47% vs. 31%, p = 0.04).The JOA scores were comparable between the two groups preoperatively, postoperatively, and at the final follow-up.

Comparisons of radiographic parameters between the two groups
Radiographic parameters of the two groups at different time points are summarized in Table 3, and illustrated in Fig. 2. All these data was measured by the two spine fellows.The interrater agreement of the parameter measurements was excellent with an ICC of 0.907, (95% CI 0.822-0.950).The Over-distraction group had a significantly smaller preoperative index disc height (4.5 vs. 5.2 mm, p < 0.001), but higher postoperative index disc height (7.7 vs. 6.6 mm, p < 0.001) and local Cobb angle (9.8° vs. 7.7°, p = 0.04) than the No-distraction group.However, at the final follow-up, the index disc height (4.8 vs. 4.5 mm, p = 0.35) and local Cobb angle (5.2° vs. 5.0°, p = 0.86) was similar between the two groups.All the other radiographic parameters except postoperative cSVA (25.8 vs. 19.8mm, p = 0.03) were comparable between the two groups preoperatively, postoperatively, and at the final follow-up, respectively and was showed at Table 4 The ROC curve of the prediction model of RASP developed from the multivariate logistic regression analysis is shown in Fig. 3, and the AUC = 0.815 (95% CI 0.744-0.887).This prediction model of RASP development has good efficacy.Over-distraction and multilevel fusion can cause higher risk of RASP progression in ACDF.

Discussions
Porous tantalum cages and polyetheretherketone(PEEK) cages were widely applied for ACDF.Porous tantalum cages have been reported similar biomechanical properties to that of cancellous bone, which allows good load transfer and minimizes the stress-shielding effect 3 .PEEK is chemically inert and does not allow for protein absorption and promotion of cell adhesion and bone contact when compared to titanium.Both TM cages and PEEK cage resulted in high fusion rate in cervical spine and lumbar spine.However, higher cage subsidence rate in TM cages than PEEK cages was revealed 2 .Therefore, we included patients who received ACDF with TM cages or PEEK cages in this study, and the overall fusion rate (88%) was consistent with prior reports [20][21][22] .Distraction of the intervertebral disc space allows better visualization when removing the disc materials and posterior osteophytes.However, over-distraction with excessive force can result in injuries to the facet joints at the index level 23 .Kirzner et al. 24 reported that over-distraction of the facet joint of ≥ 3 mm is associated with worse functional outcomes and pain scores in patients with traumatic cervical injuries treated with ACDF.Furthermore, an excessive distraction force might increase the pressure of the adjacent discs and the stress of  25 investigated the influences of the height of disc arthroplasty on cervical biomechanics using finite element study.Protheses of ≥ 2 mm of the index disc height significantly increased the adjacent intradiscal pressure, adjacent facet joint forces, and bone-implant interface stresses of the protheses, as compared to prostheses of < 2 mm of the index disc height.Interestingly, with or without excessive distraction, our results showed that the index disc heights in both groups had collapsed to a similar degree at the final follow-up (Fig. 2B).The physiologic tension of surrounding musculo-ligamentous structures might play a role in determining the final index disc height in ACDF with grafts/cages.On the other hand, Aryan et al. 26 proposed relaxing the distraction force after discectomy because they showed that the same degree of distraction could be achieved with 20N less of initial forces after removal of intervertebral discs.Since excessive distraction force might interfere the physiologic tension and affect the selection of graft/cage size, we suggested releasing the distraction force during graft/cage size trials to avoid selecting over-size grafts/cages based on the results of this study.Risk factors for the development of ASP identified in prior studies include young age, high T1 slope, preexisting disc degeneration, disruption of adjacent soft tissue, plate placement close to the adjacent disc, and poor

Figure 2 .
Figure 2. A 41-year-old female suffered from severe neck pain with bilateral hands numbness for more than one year.2a.C-spine lateral view done before the operation, which showed C4-5-6 HIVD and spondylosis.2b.Postoperative C-spine lateral view showed C4-5-6 ACDF with PEEK cage was done.2c.Well fusion without obvious RASP at 1 year after the operation.Clinical symptoms improved significantly.2d.Patient complained posterior neck pain with left arm radiation pain and numbness over C7 dermatome for 3 months.C-spine lateral view showed adjacent segment disc degeneration.This patient was classified into the CASP group.

Figure 3 .
Figure 3. Receiver operator characteristic (ROC) curve analysis of the model for predicting radiological adjacent segment pathology (RASP) developed from multivariate logistic regression analysis.The area under the ROC curve AUC = 0.815 (95% CI 0.744-0.887).
57 females) implanting with 67 levels of TM cages and 139 levels of PEEK cages were included in this study.For all patients, the mean age at the time of surgery was 53.7 years (range 31-78 years), and the mean follow-up length was 32 months (range 24-105 months).(Table2)Preoperativediagnoses included herniation of intervertebral disc (HIVD), spondylosis with osteophyte formation, and OPLL.Successful fusion was achieved in 88% (182/206) of the implanted levels.The overall incidence of cage subsidence was 36% (75/206).RASP was observed in 34% (49/145) of the patient; however, only 7 of the patients developed symptoms making the incidence of CASP = 5% (7/145).

Table 3 .
Comparison of outcomes between the Over-distraction and No-distraction groups.*Mann-Whitney U-test.† Chi-square test.Age, follow-up length, and JOA score were presented as mean ± standard deviation.M: male; F: female; RASP: radiological adjacent segment pathology; CASP: clinical adjacent segment pathology; JOA score: Japanese Orthopedic Association score. Over-
the adjacent structures.Yuan et al.

Table 5 .
Univariate and multivariate analysis for risk factors of RASP.RASP: radiological adjacent segment pathology; CI: confidence interval; OR: odds ratio.